Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus

Abstract

Central testosterone aromatization is required for the activation of both appetitive (ASB) and consummatory (CSB) male sexual behavior in Japanese quail. There are two major clusters of aromatase immunoreactive (ARO-ir) cells in the rostral forebrain; these outline the nucleus preopticus medialis (POM) and the nucleus striae terminalis (BST). We investigated the role of these nuclei in the regulation of ASB and CSB. Appetitive male sexual behavior was measured with the use of a learned social proximity procedure that quantified the time spent by a male in front of a window with a view of a female who was subsequently released into the cage, providing an opportunity for CSB. Males first acquired the response and then received bilateral electrolytic lesions aimed at the POM or BST, followed by retesting for ASB and CSB. Brain sections were stained for ARO-ir, and lesions to the two ARO-ir cell groups were quantitatively characterized. Lesions damaging the POM completely abolished CSB and also significantly decreased ASB. Lesions of the rostral BST had no effect on ASB, but moderately decreased CSB. Detailed anatomical analysis revealed that lesions of a subdivision of the POM just rostral to the anterior commissure specifically impair CSB, whereas lesions that are more rostral to this subdivision induce a severe deficit in ASB. These data indicate that different subregions of the POM regulate ASB and CSB in a somewhat independent manner, whereas the BST is only important in the regulation of CSB.

Fig. 1.

Schematic drawings of coronal sections through the quail brain illustrating the distribution of aromatase-immunoreactive cells in the medial preoptic nucleus (POM) and in the bed nucleus striae terminalis (BST)/nucleus accumbens (n. Ac.). Plates are arranged in a rostral to caudal order from the top to the bottom.

Fig. 2.

Photomicrographs illustrating the extent of a typical lesion of the POM (A–C) and of the rostral part of the BST (D, E) as seen in Nissl stain (C, E) and in sections stained by immunocytochemistry for aromatase (A, B, D). A, Lesion in the dorsal part of the rostral POM as illustrated in sections stained for aromatase. B, Higher magnification of the box inA showing the remaining aromatase-immunoreactive cells in the ventral part of the POM. C, Lesion in the caudal part of the POM at the level of the anterior commissure (CA) from a Nissl-stained section. D, Lesion of the rostral BST as seen in a section stained for aromatase.E, Adjacent section illustrating the same lesion after staining for Nissl material. This lesion of the BST partly destroys the group of aromatase-immunoreactive cells located dorsal to the commissure (BST proper) but also extends to a cell group just ventral to the lateral ventricles that is identified as the nucleus accumbens in the stereotaxic atlas of the chicken brain (Kuenzel and Masson, 1988). Scale bar (shown in E): A, C, D, E, 1 mm; B, 250 μm. FPL, Fasciculus prosencephali lateralis (lateral forebrain bundle);LV, lateral ventricle; VIII, third ventricle.

Fig. 3.

Reconstruction of the volumes (means and SEM) of the electrolytic lesions (A) and of the volumes of the POM (B), rostral BST (C), and caudal BST (D) in the four experimental groups. When the lesion actually destroyed a part of a given nucleus (POM in the In POMgroup and Rostral BST in the In BSTgroup), the corresponding bar has been divided into ahatched bar that indicates the volume of the nucleus remaining after lesion and an open bar that indicates the total extrapolated volume that would be occupied by the nucleus if no lesion were present. Experimental groups were compared two by two by Fisher’s PLSD tests whose results are indicated at thetop of the bars as follows: *p < 0.05 by comparison with the CX+T group and #p < 0.05 by comparison with the CX group. Parentheses around a symbol indicate that the corresponding general ANOVA comparing the four groups did not detect a significant effect, so that results of Fisher’s PLSD tests can only be considered as indicative (see Results for more detail).

Fig. 4.

Effects of lesions of the POM or BST for one of the measures of appetitive (Time at Window) and for one of the measures of consummatory (Cloacal Contact Movements) male sexual behavior in castrated male quail treated with exogenous testosterone. Data for CX birds not treated with testosterone are also illustrated. The data shown (means ± SEs) represent the acquisition of behaviors during the eight preoperative tests (Pretests) and then the effects of the experimental manipulations observed during the nine postoperative tests (Tests) in the four experimental groups.

Fig. 5.

Means of the behavioral scores for all the behavioral measures taken for both appetitive and consummatory male sexual behavior observed in the four experimental groups during the postoperative phase of the experiment. Data presented are the means ± SEs of the mean of the behavioral frequencies or of time spent in front of the window during the nine separate tests. For each dependent variable, results corresponding to the four experimental groups were compared by a one-way ANOVA, and these results are summarized in the bottom right panel (F values, df, and associated probabilities; ***p < 0.001). Experimental groups were then compared two by two by Fisher’s PLSD tests whose results are indicated at the top of the bars.

Fig. 6.

Relations between the two measures of appetitive sexual behavior and the two measures of consummatory sexual behavior in birds bearing a lesion of the POM and in their control group (CX+T). Correlation coefficients associated with the four regression lines indicated in the figure are not significant (p > 0.05) except for CCM Frequency versus Look Frequency in the In POM group (r = 0.536; p= 0.012). These data clearly illustrate the nearly complete inhibition of consummatory sexual behavior but the quite variable inhibition of appetitive sexual behavior in the lesioned group.

Fig. 7.

Factor analysis of the dissociation between appetitive and consummatory aspects of male sexual behavior in birds bearing a POM lesion and of the relationship of the behavioral deficit to the lesion location within POM. A, Results of the factor analysis of the correlations between behavioral measures and the associated scores of the POM lesion. The figure presents a three-dimensional plot of the factor loadings relative to the first three factors extracted by the analysis that explain 74% of the total variance present in the data. Four clusterings of scores associated with the lesion scores at four different levels are apparent. The position of the behavioral scores for the measures of appetitive and consummatory male sexual behavior is also plotted. B, C, Projection in two different planes defined by vectors 1 and 2 or 1 and 3 of the factor loadings for the different variables. In both cases, four clusters of data points representing the lesion scores at the four different rostrocaudal levels are clearly present. The two measures of consummatory sexual behavior are clearly associated with lesion scores at Level 3, whereas the measures of appetitive sexual behavior (TIME, LOOK, and ENTR) are located in a position intermediate between lesion scores at levels 2 and 3.

Fig. 8.

A, Mean ± SE of the behavioral scores (frequencies of behavior or time at window) computed for three subgroups of birds bearing a POM lesion (In POM group) defined by the presence of appetitive sexual behavior and a low level of consummatory sexual behavior (ASB+/CSB+), by the presence of appetitive sexual behavior and the complete absence of consummatory sexual behavior (ASB+/CSB−), or by the strong inhibition of appetitive sexual behavior and the complete absence of consummatory sexual behavior (ASB−/CSB−). Data were analyzed by one-way ANOVA (see Results) followed by Fisher’s PLSD tests comparing groups two by two. The results of the statistical analyses are illustrated at the top of the bars as follows: *p < 0.05 by comparison with ASB+/CSB+ subgroup and #p < 0.05 by comparison with ASB+/CSB− subgroup. B, Means of the lesions scores observed in eight quadrants of the POM (four quadrants on each side of the POM) at the four rostrocaudal levels in the three subgroups of birds defined by their behavior. Data were analyzed by a separate one-way ANOVA for each rostrocaudal level (see Results) followed by Fisher’s PLSD tests comparing groups two by two. The results are shown at the top of the bars as follows: *p < 0.05 by comparison with ASB+/CSB+ subgroup and #p < 0.05 by comparison with ASB+/CSB− subgroup. Parentheses around a symbol indicate that the corresponding general ANOVA comparing the three subgroups did not detect a significant effect, so that results of the Fisher PLSD tests can only be considered as indicative.

Fig. 9.

Comparison of the behavioral responses observed in castrated birds treated or not treated with testosterone and in birds with a lesion in POM or BST when tested for appetitive sexual behavior after the completion of the nine postoperative tests. In this case, the cage adjacent to the main chamber either contains or does not contain a stimulus female. In all groups, in the absence of the females the time spent in front of the window and the frequency of looks through the window decreased. At the same time, there was an increase in the number of times that birds entered the test area in front of the window relative to tests when the female was present.

Fig. 10.

Effects of testosterone treatment and of a lesion in the POM on the frequency of rhythmic cloacal sphincter muscles movements (RCSM), on the number of bouts of RCSM, and on the latency to initiate RCSM in the absence (Pretest) or presence (Test) of a stimulus female. Fisher’s PLSD tests were performed to compare the behavior of the three groups of birds in the absence (Pretest) and presence (Test) of the female. The results are reported by symbols at thetop of the corresponding bar in the graph (*p < 0.05 by comparison with the CX group; #p < 0.05 by comparison with the CX+T group).